Environmental Experience and Plasticity of the Developing Brain E-Book

• Herausgeber: John Wiley & Sons
• Kategorie: Wissenschaft und neue Technologien
• Sprache: Englisch

Seitenzahl: 522

Veröffentlichungsjahr: 2016

Beschreibung

Environmental Experience and Plasticity of the Developing Brain goes beyond the genetic basis of neurodevelopment. Chapters illuminate the external factors that can dramatically impact the brain early in life and, consequently, the eventual accomplishment of developmental milestones and the construction of adult behavior and personality. Authored and edited by leaders in this rapidly growing field, Environmental Experience and Plasticity of the Developing Brain not only surveys preexisting literature on the effects of environment versus genetics, but also discusses more recent studies on the impacts of neurodevelopment in terms of maternal stimulation, environmental enrichment and sensory deprivation. The book also includes key examples of environmental impacts on preexisting genetic syndromes leading to developmental disabilities. Focus is also given to the consequences of early adverse experience in primates, as well as neurobiological and behavioral consequences in institutionalized human children and the reversibility of such consequences. Environmental Experience and Plasticity of the Developing Brain encompasses a broad area of research in the field of developmental neurobiology and offers a unique combination of different examples of environmental factors affecting brain development and behavior.

Leseprobe

Table of Contents

Cover

Dedication

Title Page

Copyright

List of contributors

Chapter 1: Environmental enrichment and brain development

Introduction: critical periods and experience-dependent plasticity in brain circuits

Optimization of environmental stimulation: environmental enrichment

Environmental enrichment and visual system development

Concluding remarks

References

Chapter 2: Epigenetic control of visual cortex development and plasticity

Introduction

Overview of chromatin modifications

Epigenetics and brain plasticity

Epigenetic control on visual system development

Future directions

Acknowledgments

References

Chapter 3: Gene–environment interactions in the etiology of psychiatric and neurodevelopmental disorders

How animal models help us study human brain disorders

Genetic models for complex brain diseases

Behavioral outcomes from environmental modulation

Components of environmental enrichment

Molecular changes in response to environmental modulation

Environment, BDNF, stress, and depression

Epigenetics and environmental influence

Overview of Rett syndrome

Genetic sources of phenotypic variation in Rett syndrome and other brain disorders

The functions of MeCP2

Can disease progression in Rett syndrome be prevented?

Regulation of

Bdnf

and

Crh

by MeCP2

Effects of environmental enrichment in

Mecp2

mutant mice

Summary

References

Chapter 4: Critical periods and neurodevelopmental brain disorders

Introduction

Developmental aspects of NDDs

Brain development and critical periods

Dysregulation of brain development in NDDs: a framework for misregulated timing

Potential mechanisms underlying critical period dysregulation in NDDs

Corrective strategies for NDDs: genetic and pharmacological interventions

Syndrome-specific molecules or common signalling hubs? Targets for future pharmacotherapeutic interventions

Dysregulated critical period framework as a unifying hypothesis for prominent NDD theories

Implications of misregulated critical periods and future directions

Acknowledgments

References

Chapter 5: Maternal care and DNA methylation

Introduction

DNA methylation

DNA methylation and regulation of gene expression

Reversibility of DNA methylation

DNA methylation changes triggered by differences in maternal care in the

nr3c1

gene

Molecular conduit between experience and DNA: signaling cascade leading from maternal care to epigenetic programming

Reversibility of epigenetic programming by maternal care

Epigenetic programming by early life experience in humans; rRNA genes are hypermethylated in suicide victims who were abused as children

The response to early life adversity is broad and involves several gene networks

System-wide responses to maternal deprivation; the impact of rearing differences in nonhuman primates

Natural disasters as a model to study the impact of maternal stress on child DNA methylation

Summary

Acknowledgments

References

Chapter 6: Neurobiology and programming capacity of attachment learning to nurturing and abusive caregivers

Introduction

Infant attachment

Neurobiology of attachment learning

Neurobiology of abusive attachment learning

Maternal control of attachment

Attachment and epigenetic programming

Functional consequences

Concluding remarks

Acknowledgments

References

Chapter 7: Early environmental manipulations and long-term effects on brain neurotrophin levels

Introduction

Long-term effects of infantile stimulation on brain plasticity

Neurotrophins and brain plasticity

Neurotrophins as transducers of early experiences

Neurotrophins as transducers of stressful events

Windows of opportunity: environmental enrichment as a means to achieve a fine-tuning of brain plasticity and of social and emotional behavior

Epigenetic changes as one mechanism linking early experiences and adult neurobehavioral profile

Conclusion

References

Chapter 8: Effects of genes and early experience on the development of primate behavior and stress reactivity

Introduction

Assessment of infant behavior and stress reactivity

Influence of naturally occurring variation in maternal style on offspring behavior and stress reactivity

Main genetic effects on the development of infant behavior and stress reactivity

Summary and conclusions

References

Chapter 9: Institutional deprivation and neurobehavioral development in infancy

Introduction

Cognition

Emotion

Behavior

Brain development

Electrophysiology

HPA activity

Genetic moderation and epigenetics

Evidence for sensitive periods

Factors modifying postinstitutional outcomes

Interventions and evidence for plasticity

Comparisons with other forms of adversity

Individual differences and resilience

Conclusions

Acknowledgments

References

Chapter 10: Impact of infantile massage on brain development

Introduction

Early intervention programs and infant massage

Infant massage as a model of environmental enrichment

Summary and conclusions

References

Index

End User License Agreement

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Guide

Cover

Table of Contents

Begin Reading

List of Illustrations

Chapter 1: Environmental enrichment and brain development

Figure 1.1 Critical period (CP) for ocular dominance plasticity in the rat visual cortex. (a) Schematic representation of the time course of CP for ocular dominance plasticity in the rat, which peaks around postnatal day (P) 21 and is definitively closed by the age of P45. (b) Single unit recordings from the primary visual cortex allow classification of neurons with respect to their ocular preferences: in a typical recording from a nondeprived animal (light cyan columns), cells in class 1 are activated exclusively by the contralateral eye, cells in class 7 are activated exclusively by the ipsilateral eye, neurons in classes 2–3 and 5–6 are activated to varying degrees by both eyes, and neurons in class 4 respond equally to both eyes. Following closure of the contralateral eye from 1 week during the CP, cells become much more responsive toward the ipsilateral open eye, at the expense of the deprived eye (dark cyan columns). (See insert for color representation of this figure.)

Figure 1.2 Critical periods across brain functions in humans. The picture represents a schematic of the critical period time course for acquisition of binocular vision, language learning, and adequate peer social skills in children. Different functions display different time courses, both in terms of total duration of the heightened sensitivity window and concerning the age of onset and closure of the potential for plasticity. In the three curves, levels of plasticity have been normalized to the peak. (See insert for color representation of this figure.)

Figure 1.3 Environmental enrichment and visual system development acceleration: a three phases model. The Figure depicts an interpretative framework of the data regarding EE effects on the developing visual system. Three consecutive temporal phases are differently controlled by the richness of the environment: (I) a prenatal phase in which the mother mediates the influence of the environment through placental exchanges with the fetus, leading to an accelerated anatomical retinal development that is mostly due to increased levels of IGF-1; (II) an early postnatal phase in which enhanced maternal care received by EE pups stimulates the expression of experience-dependent factors in the visual system, resulting in an early increase of BDNF and IGF-1 in the retina and the visual cortex; this guides the accelerated maturation of retinal ganglion cells (RGCs) observed in EE pups and, through an increased GABAergic inhibitory transmission, triggers a faster visual cortex development; and (III) a third and final phase in which the autonomous interaction of the developing pup with the enriched environment further increases cortical IGF-1, which promotes the maturation of the GABAergic system, also leading to an acceleration in visual acuity maturation. Continuous lines represent well-documented interactions between boxes; dashed lines indicate likely interactions in the context of visual cortex development requiring further experimental characterization. (See insert for color representation of this figure.)

Figure 1.4 Prenatal enrichment modulates retinal development in the fetus. The Figure shows a possible explicative model for the effects elicited by maternal enrichment during pregnancy on retinal development. Increased levels of physical exercise in gestating dams lead to higher amounts of circulating IGF-1 in the maternal blood stream, stimulating the supply of nutrients transferred to the fetus through the placental barrier. The enhancement in glucose and placental lactogens received by the fetus stimulates the autonomous production of IGF-1 in his tissues, with an increased expression detectable in the ganglion cell layer of the retina. IGF-1, in turn, stimulates the maturation of retinal circuitries. The photographs depict two examples of one enriched (left) and one nonenriched (right) retinal sections immunostained for double cortin, which labels migrating cells and is a good marker of the temporal and spatial distribution of neural progenitors during the early developmental stages of the rat retina. Reprinted from Sale et al., 2012. (See insert for color representation of this figure.)

Figure 1.5 Exposure to enriched conditions promotes recovery of visual functions in adult amblyopic rats. (a) Experimental amblyopia is easily induced in juvenile rats by imposing an artificial closure of one eye through lid suture (monocular deprivation [MD]), started at the peak of the critical period (postnatal day 21) and maintained until the animals reach the adult age (around P70). Then, reverse suture (RS) is performed, consisting in the reopening of the long-term deprived eye and simultaneous closure of the fellow eye, in order to force the animals to use their lazy eye. After RS, the animals are divided in two groups, one left undisturbed under standard-rearing conditions, the other one being transferred to an enriched environment setting. (b) Rearing adult amblyopic rats in an enriched environment for 3 weeks leads to a complete recovery of visual functions, in terms of visual acuity, binocularity, and stereopsis. (See insert for color representation of this figure.)

Figure 1.6 Visual perceptual learning induces long-term potentiation in the primary visual cortex. (a) A modified version of the visual water box task (Prusky et al., 2000; Cancedda et al., 2004) was used to induce visual perceptual learning in a group of adult rats that were first trained to distinguish a low 0.117 cycles per degree (c/deg) spatial frequency (SF) grating (reference grating) from a 0.712 c/deg SF grating (test grating) (right panel) and then learned to distinguish the two gratings when they became more and more similar to each other. A group of control animals was trained to distinguish the reference grating from a homogeneous gray (left panel). After training, LTP from layer II–III of V1 slices was occluded in PL animals compared to controls, at the level of both vertical (blue arrow) and horizontal (red arrow) connections. Sample traces from PL and control slices 5 minutes before (thin line) and 25 minutes after (thick line) induction of LTP are shown. (b) Visual perceptual learning is specific for stimulus orientation. The graphs show daily discrimination threshold values obtained in PL animals trained in discriminating first horizontal gratings and then tested with vertical. After the orientation change, the animals displayed a marked impairment in their discrimination abilities. Reprinted from Sale et al., 2012. (See insert for color representation of this figure.)

Chapter 2: Epigenetic control of visual cortex development and plasticity

Figure 2.1 Sketch of histone post-translational modifications induced by visual experience on miR212/132 gene. (See insert for color representation of this figure.)

Chapter 3: Gene–environment interactions in the etiology of psychiatric and neurodevelopmental disorders

Figure 3.1 Positive and negative environmental experiences affect epigenetic markings and gene expression.

Figure 3.2 Role of genetic background in epigenetic regulation of gene expression that may be involved in psychiatric disorders.

Chapter 4: Critical periods and neurodevelopmental brain disorders

Figure 4.1 Developmentally regulated time windows in the Fmr1-KO mouse model. Several morphological and functional impairments in synapse properties are observed in the somatosensory cortex and specifically the barrel region of the Fmr1-KO model for Fragile X syndrome (FXS) (Nimchinsky et al., 2001; Bureau et al., 2008; Gibson et al., 2008; Cruz-Martin et al., 2010; Harlow et al., 2010). Many of these functional alterations are transient, occurring only during restricted periods of early postnatal development. Another developmentally regulated phenotype is spine morphology in layer 5 pyramidal neurons, where the alteration disappears at P28 but reappears in later adulthood around P75 (Nimchinsky et al., 2001; Galvez and Greenough, 2005). (Taken from Meredith et al., 2012.)

Figure 4.2 Regulation of developmental synaptic phenotypes and potential alteration in neurodevelopmental brain disorders (NDDs). (Left) Developmental profiles of synaptic phenotypes illustrating neurotypical development (top), developmental delay (middle), and precocial phenotypic onset (bottom). Gray bars indicate critical periods for phenotype plasticity. (Right) An example of a developmentally regulated synapse phenotype, spine morphology with longer, thinner filopodia-like spines observed in the immature state and shorter, stubbier spines in the mature state. Predicted phenotypic differences for developmental delay and precocial onset differences illustrated at phenotypic peak for neurotypical profile (black curves in lefthand panel). (Adapted from Meredith et al., 2012.) (See insert for color representation of this figure.)

Figure 4.3 Many NDD-associated and linked genes function at the synapse to alter spine morphology. Many monogenic syndrome-associated genes (red) function at the synapse, illustrated here postsynaptically, to mediate changes in spine morphology via small GTPase-mediated signalling pathways and F-actin in response to synaptic activation (receptors highlighted in green). Abbreviations: AMPA, 2-amino-3-(3-hydroxy-5-methyl-isoxazol-4-yl) propanoic acid receptor; Cdc42, cell division cycle 42; CYFIP, cytoplasmic binding partner of Fragile X protein; FMRP, Fragile X Mental Retardation Protein; LimK1, LIM domain kinase 1; mGluR5 metabotropic glutamate receptor subunit 5; NMDA, N-Methyl-D-aspartic acid or N-Methyl-D-aspartate Receptor; OPHN1, oligophrenin-1; PAK, serine/threonine-protein kinase; Rac1, ras-related C3 botulinum toxin substrate; RhoA, ras homolog gene family, member A; MLCP, Myosin light-chain phosphatise. (Modified from Kroon et al., 2013.) (See insert for color representation of this figure.)

Figure 4.4 Illustrated hypothesis of how dysfunction of NDD-associated genes may dysregulate critical periods. A critical period is shown here as the timeframe between ``1'' and ``2'' (a). In this scenario, the critical period is caused by changing genetic expression (blue bar), such as expression of the GABA-synthesising enzyme, GAD65. Expression of the NDD gene (red bar) during neurotypical development is constant before, during, and after the critical period. Expression of genes that determine the dynamics of the critical period does not directly regulate the ``NDD gene.'' Rather, the NDD gene role can indirectly regulate the critical period via its interaction with molecules that mediate synaptic changes during the critical period; for example, expression of GABAergic receptor subunits necessary to mediate synaptic inhibition. FMRP is able to interact with other 800 different mRNA targets in the adult brain, including many proteins with synaptic function and localization (Darnell et al., 2011). Hence dysfunction of the NDD gene can lead to an impaired critical period by indirect regulation. (b) Increased NDD gene expression changes during a restricted developmental stage (red curve) and directly regulates the occurrence of a critical period, independent of external factors. Such dynamic patterns of upregulated ``NDD gene'' expression, coincident with timing of thalamic and cortical critical periods, occur for many genes including Fmr1, neurofibromin (NF1), and ubiquitin-protein ligase E3A (UBE3A) (Figure 3 Kroon et al., 2013, Allen developing mouse brain atlas: http://developingmouse.brain-map.org). Therefore, dysfunction of the NDD gene causes the critical period to be absent completely. (c) In both scenarios, the NDD gene is necessary for the phenotypic change that takes place during the critical period (``WT'' vs. ``KO''), represented here by maturation of spine morphology. (Figure taken from Kroon et al., 2013.) (See insert for color representation of this figure.)

Figure 4.5 Framework of dysregulated critical periods and time windows during brain development as unifying theory for temporal aspects of mechanisms underlying many NDDs of ID and ASD, and prominently illustrated in this article with the Fmr1-KO mouse model for Fragile X syndrome. The three prominent hypotheses for the neurobiological bases of NDDs are shown, namely (1) altered connectivity at short- and long-range distances between neurons, (2) a relative imbalance between excitation (E) and inhibition (I) within brain circuitry, and (3) hyperexcitability of neurons with specific networks in the brain. Neuronal connectivity and both excitatory and inhibitory synaptic strength undergo heightened plasticity during early critical periods in the brain. It is likely that dysregulated phenotypes, such as an imbalance in the levels of synaptic excitation and inhibition, first arise during these critical periods in NDD models. Therefore, the use of known critical periods for cortical and hippocampal circuits may predict when these phenotypes first occur and how long they remain. (See insert for color representation of this figure.)

Chapter 5: Maternal care and DNA methylation

Figure 5.1 DNA methylation and demethylation reactions. DNA methylation reactions require the methyl donor SAM and are catalyzed by DNMT. Demethylation was suggested to be catalyzed by a bona fide demethylase (MBD2-demethylase), which removes a methyl group from DNA and releases it as methanol. Alternative mechanisms for demethylation involve either hydroxylation of the methyl group by TET enzymes or deamination by deaminase enzymes followed with repair. The methyl group is further modified to hydroxymethylcytosine by TET enzymes. Methylation at critical 5' regulatory sites blocks transcription (X) while it is unclear whether hydroxylation might relieve this repression.

Figure 5.2 Epigenetic programming by maternal care. Maternal care causes activation of serotonin (5-HT) receptors, increases cAMP activation of protein kinase A followed by activation of NGFIA, which interacts with the

nr3c1

promoter and recruits chromatin modifying enzymes and MBD2/demethylase. Increased LG results in decreased methylation of DNA (CH3), increased histone acetylation (AC), and increased gene expression. The DNA methylation reaction is potentially reversible: histone deacetylase inhibitor TSA causes demethylation and activation of the gene, while methionine causes increased methylation and silencing of the gene. (See insert for color representation of this figure.)

Chapter 6: Neurobiology and programming capacity of attachment learning to nurturing and abusive caregivers

Figure 6.1 This schematic represents pups' transitions in attachment learning with odor-0.5 mA shock conditioning. Pups younger than PN10 have robust attachment learning during a sensitive period. Older pups readily learn fear, although maternal presence through social buffering enables the reinstatement of the sensitive period (PN, postnatal day; NE, norepinephrine; CORT, corticosterone; LC, locus coeruleus).

Figure 6.2 DNA methylation. (a) DNA in the nucleus is wrapped around histone proteins, forming what is referred to as chromatin. (b) DNA methylation can occur at cytosine residues of cytosine-guanine (CG) dinucleotides that are clustered within gene regulatory regions. DNA methylation is an epigenetic mechanism typically associated with gene suppression, as methyl groups can either interfere with the binding of transcription factors necessary to promote gene transcription and/or recruit repressor proteins that promote a compact chromatin state not permissive to gene transcription.

Figure 6.3 Summary of maltreatment-induced DNA methylation alterations that we have observed in the brain of adult male (left panel) and female (right panel) rats (3 months removed from the infant experiences).

Increased

,

decreased

, or

no change

refers to methylation changes in maltreated rats in comparison to normal (nurturing) care controls. Changes in methylation are for DNA associated with important regulatory regions of the

Bdnf

gene (

Bdnf

I or IV). (Figure is recreated from data in Blaze et al., 2013 and Roth et al., 2009, 2014.)

Figure 6.4 (a) Effects of pairing ethanol (EtOH) with shock at 8 days of age on adult EtOH preference (% preferring EtOH over water). Early odor-shock conditioning during the sensitive period had long-term consequences as determined in the two bottle preference test. Adults were given a choice of dilute EtOH (1% v/v) or water for 3 days and then the concentration was increased every 3 days (1%, 3%, 5%, 7%). The paired EtOH-shock animals showed a strong preference for alcohol over water when given free choice, upward of 85–99%. The unpaired shock-EtOH odor animals showed increased consumption compared to the odor-only animals but significantly less that the paired animals, except at the highest concentration. (b) These data are from the 3 days of testing. At the lowest concentration of EtOH (1%), the paired animals showed the greatest intake compared to unpaired odor-shock or EtOH alone. For the highest concentration, unpaired shock-odor as well as shocked paired with odor enhanced compared to controls. ** p < .01 from odor only; *p < .05 from odor only; ∧p < .05 from unpaired EtOH-shock.

Figure 6.5 Summary of outcomes associated with being raised in either abusive or nurturing caregiving environments.

Chapter 7: Early environmental manipulations and long-term effects on brain neurotrophin levels

Figure 7.1 The mother–infant relationship is fundamental for brain and behavioral development of the offspring. The mother provides nourishment and produces a sensory-tactile stimulation that stimulates brain growth through maternal behaviors such as licking and grooming.

Figure 7.2 Stable changes in gene function might result from the interaction between the genotype and the environment leading to a specific phenotype. Neurotrophins are crucial effectors in changes in brain function deriving from external manipulations.

Chapter 8: Effects of genes and early experience on the development of primate behavior and stress reactivity

Figure 8.1 A rhesus macaque mother with her infant on Cayo Santiago, Puerto Rico. (Photo: Sean Coyne.) (See insert for color representation of this figure.)

Figure 8.2 Social play (rough-and-tumble) between two rhesus macaque juveniles on Cayo Santiago, Puerto Rico. (Photo: Sean Coyne.) (See insert for color representation of this figure.)

Figure 8.3 A rhesus macaque infant on Cayo Santiago, Puerto Rico. (Photo: Sean Coyne.) (See insert for color representation of this figure.)

Chapter 9: Institutional deprivation and neurobehavioral development in infancy

Figure 9.1 Percentage of children adopted from institutional or foster care with CBCL scores of >61 in each domain. (a) Children adopted before 24 months of age. (b) Children adopted after 24 months of age. Regardless of type of care, children adopted later were more likely to express elevated behavior problems. Main effects of institutional care were only noted for attention and social problems. Adapted from Gunnar & van Dulmen, 2007. (See insert for color representation of this figure.)

Figure 9.2 Error-related negativity averaged across Flanker and Go-NoGo (counter-balanced) tasks for postinstitutionalized (PI) children and non-adopted (NA) children raised in families comparable to those who adopt children internationally. Bars reflect standard error of the mean. Adapted from Loman et al., 2013.

Figure 9.3 Predicted diurnal cortisol across the day for postinstitutionalized children among high- and low-quality social care in institutions. Graphs depict 1 SD above and below the mean of the social care construct as an illustration of high- and low-quality social care. Kalsea J. Koss, Camelia E. Hostinar, Bonny Donzella, Megan R. Gunnar 2014, Figure 2. Reproduced with permission of

Psychoneuroendocrinology

, Elsevier.

Figure 9.4 Potential effects of early institutional care. These effects are not specific to institutional care, as they may also follow other forms of early adversity. The duration of institutionalization increases the risk of these outcomes. (See insert for color representation of this figure.)

Chapter 10: Impact of infantile massage on brain development

Figure 10.1 Schematic representation of the massage protocol used in Guzzetta et al., 2009, based on the one proposed by Tiffany Field. The protocol consists of 2 weeks of intervention with 1-day pause, with three 15-minute sessions per day. Each session is composed of two 5-minute tactile stimulations and one 5-minute kinesthetic stimulation.

Figure 10.2 Schematic representation of the results from Guzzetta et al., 2009. On the left side the time of intervention and the time of assessments are indicated. In the insets, main results are shown. T1-T0: Difference between premassage and postmassage assessment of VEP N300 latency and maximum EEG interburst interval. Boxes indicate median (black horizontal line), interquartile values, and range. Massaged infants show larger differences between T1 and T0, which are statistically significant from those in controls. T2 and T3: Behavioral visual acuity measured in cycles per degree (c/deg) by means of the Vital-Durand Acuity Cards at 3 and 7 months corrected age. Bars indicate mean values and SEM. Visual acuity in massaged infants is significantly higher than in controls at 3 months, but the difference is no longer present at 7 months.

To my Mentors, Teachers, and Friends, Prof. Lamberto Maffei and Prof. Floriano Papi, as a sign of respect and gratitude.

Environmental Experience and Plasticity of the Developing Brain

EDITED BY

Alessandro Sale

Copyright © 2016 by John Wiley & Sons, Inc. All rights reserved

Published by John Wiley & Sons, Inc., Hoboken, New Jersey

Published simultaneously in Canada

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List of contributors

Enrico Alleva

Section of Behavioral Neurosciences, Department of Cell Biology and Neurosciences, Istituto Superiore di Sanità, Rome, Italy

Gordon A. Barr

Department of Anesthesiology and Critical Care Medicine, The Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, USA; Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA

Nicoletta Berardi

Department of Neuroscience, Psychology, Drug Research and Child Health NEUROFARBA, University of Florence, Florence, Italy

Giovanni Cioni

Department of Clinical and Experimental Medicine, Pisa University, Pisa, Italy; Department of Developmental Neuroscience, Stella Maris Scientific Institute, Pisa, Italy

Francesca Cirulli

Section of Behavioral Neurosciences, Department of Cell Biology and Neurosciences, Istituto Superiore di Sanità, Rome, Italy

Sean P. Coyne

Department of Comparative Human Development, The University of Chicago, Chicago, Illinois, USA

Jenalee R. Doom

Institute of Child Development, University of Minnesota, Minneapolis, Minnesota, USA

Megan R. Gunnar

Institute of Child Development, University of Minnesota, Minneapolis, Minnesota, USA

Andrea Guzzetta

Department of Clinical and Experimental Medicine, Pisa University, Pisa, Italy; Department of Developmental Neuroscience, Stella Maris Scientific Institute, Pisa, Italy; SMILE Lab, Stella Maris Scientific Institute, Pisa, Italy

Anthony J. Hannan

Florey Institute of Neuroscience and Mental Health, University of Melbourne, Parkville, Australia; Department of Anatomy and Neuroscience, University of Melbourne, Parkville, Australia

Mari A. Kondo

Department of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA

Michael J. Lewis

Department of Psychology, Hunter College, City University of New York, Manhattan, New York, USA; Institute of Human Nutrition, Columbia College of Physicians and Surgeons, Columbia University, New York, New York, USA

Dario Maestripieri

Department of Comparative Human Development, The University of Chicago, Chicago, Illinois, USA

Lamberto Maffei

Neuroscience Institute, National Research Council (CNR), Pisa, Italy

Rhiannon M. Meredith

Center for Neurogenomics & Cognitive Research (CNCR), VU University Amsterdam, Amsterdam, The Netherlands

Tommaso Pizzorusso

Neuroscience Institute, National Research Council (CNR), Pisa, Italy; Department of Neuroscience, Psychology, Drug Research and Child Health (NEUROFARBA), University of Florence, Florence, Italy

Elena Putignano

Neuroscience Institute, National Research Council (CNR), Pisa, Italy

Tania L. Roth

Department of Psychological and Brain Sciences, University of Delaware, Newark, Delaware, USA

Alessandro Sale

Neuroscience Institute, National Research Council (CNR), Pisa, Italy

Regina M. Sullivan

Emotional Brain Institute, Nathan Kline Institute, Orangeburg, New York, USA; Child and Adolescent Psychiatry, New York University Langone Medical Center, New York, USA

Moshe Szyf

Department of Pharmacology and Therapeutics, McGill University, Montreal, Quebec, Canada

Paola Tognini

Neuroscience Institute, National Research Council (CNR), Pisa, Italy

Chapter 1Environmental enrichment and brain development

Alessandro Sale1, Nicoletta Berardi2 and Lamberto Maffei